Download Comparison of the nutrient composition of royal jelly and

Comparison of the nutrient composition of royal jelly
and worker jelly of honey bees (Apis mellifera)
Ying Wang, Lanting Ma, Weixing Zhang, Xuepei Cui, Hongfang Wang,
Baohua Xu
To cite this version:
Ying Wang, Lanting Ma, Weixing Zhang, Xuepei Cui, Hongfang Wang, et al.. Comparison of
the nutrient composition of royal jelly and worker jelly of honey bees (Apis mellifera). Apidologie, Springer Verlag, 2016, 47 (1), pp.48-56. .
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Apidologie (2016) 47:48–56
* INRA, DIB and Springer-Verlag France, 2015
DOI: 10.1007/s13592-015-0374-x
Original article
Comparison of the nutrient composition of royal jelly
and worker jelly of honey bees (Apis mellifera )
Ying WANG , Lanting MA , Weixing ZHANG , Xuepei CUI , Hongfang WANG , Baohua XU
College of Animal Science and Technology, Shandong Agricultural University, Tai’ an, Shandong 271018, People’s
Republic of China
Received 9 December 2014 – Revised 14 March 2015 – Accepted 2 June 2015
Abstract – In this study, the chemical and mineral composition and trace elements in royal jelly (RJ) and worker
jelly (WJ) and in royal jelly on particular days (only-2-day RJ [O2d], only-3-day RJ [O3d] and only-4-day RJ [O4d])
were determined. Significant differences in levels of moisture, protein, 10-hydroxy-2-decenoic acid (10-HDA),
fructose (F) and glucose (G) were found between the RJ and WJ samples. The nutrient content was significantly
higher in samples on O2d than the O3d and O4d samples. The results of this study add to the current knowledge of
the nutritional value of RJ and WJ. These results also imply a strong relationship between nutritional effects and
polyphenism in honey bees.
chemical / composition / royal jelly / worker jelly
1. INTRODUCTION
The characteristics of organisms are considered
to be the comprehensive result of both genetics
and the environment. The honey bee is a perfect
model to explore the interaction of these two
factors. Genetic factors are decisive in sex determination in honey bees. The females (workers or
queens) are developed from fertilized eggs, and
unfertilized eggs become drones (males). Although the queen and worker have the same genotype, they differ greatly in their behavior, physiology and development (Winston 1991), and this
is most likely the result of environment factors.
Both the queen and worker larvae are fed royal
jelly for the first 3 days of that stage. The worker
larvae are subsequently fed a mixture of royal
jelly, pollen and honey, while the older queen
larvae are provided with abundant royal jelly
(Haydak 1943). The quality and quantity of larval
Corresponding author: B. Xu, [email protected]
Manuscript editor: Stan Schneider
food is believed to be the primary catalyst for the
differentiation in development (Haydak 1943;
Winston 1991). There are few reports on the
differences between royal jelly (RJ) and worker
jelly (WJ). Studies have shown that the moisture
content of RJ is lower than that of WJ (Elser
1928; Smith 1959). Sugar is another important
factor that may influence caste determination.
Asencot and Lensky (1988) found that the food
of 1- to 3-day-old queen larvae contained 12.4 %
sugars, which was approximately four times that
found in WJ. Studies have also found that adding
sugars to WJ induced larvae to become queens
(Asencot and Lensky 1985). Recent reports have
noted that caste determination in honey bees is
influenced by a 57-kDa protein in royal jelly
through an epidermal growth factor receptor
(EGFR)-mediated signaling pathway (Kamakura
2011). While these studies strongly suggest a
close relationship between food nutrients and
caste determination, we still have little knowledge
regarding the differences in chemical composition between RJ and WJ, such as the content of
proteins, lipids, 10-hydroxy-2-decenoic acid
(HDA) and mineral elements.
Chemical composition of royal jelly and worker jelly
The composition of RJ has been the subject of
investigation by numerous researchers for more
than a century (Lercker et al. 1981; cf. reviews:
Ramadan and Al-Ghamdi 2012). The content of
moisture (Sabatini et al. 2009), carbohydrates
(Asencot and Lensky 1988; Lercker et al. 1992),
proteins (Simúth 2001; Boselli et al. 2003; GarciaAmoedo and Almeida-Muradian 2007), lipids
(Lercker et al. 1992; Noda et al. 2005), 10-HDA
(Bloodworth et al. 1994; Koshio and de AlmeidaMuradian 2003; Pamplona et al. 2004) and minerals (Benfenati et al. 1986; Stocker et al. 2005;
Garcia-Amoedo and Almeida-Muradian 2007)
has been thoroughly documented. However, it is
important to note that almost all of these studies
were focused on the quality of commercial RJ
(i.e., the food of 4-day-old queen larvae). Furthermore, the food of queen larva in its cell is increasing daily, and the larva always eat the freshest
food. It is doubtful that there is any change in
the composition of the RJ that the queen larvae
is fed daily by nurse bees. This study is based on
the hypothesis that the composition of whole RJ
obtained from a cell is different from that supplied
to queen larva by nurse workers on a particular
day.
If the nutrient composition of RJ and WJ are
different, we will be forced to reexamine the relationship between nutrients and caste determination in honey bees. The aim of this study was the
systematic investigation of the chemical composition (including moisture, total protein, 10-HDA,
carbohydrates and minerals) of different-aged
samples of RJ and WJ.
49
comb for 24 h using a queen spawning controller
(Changge Jihong Beekeeping Equipment Co.,
He’nan, China). The laid-comb was then transferred to a super and the queen was kept in the
hive body. A queen excluder was used to separate
the queen from the super. After the eggs were
deposited, the 1-day-old larvae were grafted into
artificial cells using a standard royal jelly production technique (Chen et al. 2002). Every 24 h, 100
worker larvae of each colony were removed from
the cells, and the WJ were obtained using a retractable Chinese-style grafting tool. The RJ samples of particular days were divided into two portions: the whole RJ samples and the RJ samples
that the nurse bees fed the queen larvae on that
particular day (see Figure 1). A mark was made
on the surface of the artificial cells. To obtain each
day’s RJ samples, the RJ added on top of the mark
from the previous day in each cell was collected
(Figure 1). Each type of RJ sample was obtained
from 33 queen cells in each colony. Sampling was
performed on the following days: only-2-day RJ
(O2d), only-3-day RJ (O3d) and only-4-day RJ
(O4d). We collected five individual samples for
2. MATERIALS AND METHODS
2.1. Collection of RJ and WJ samples
All experiments and surveys were conducted in
the experimental apiary of Shandong Agricultural
University (Tai’ an, Shandong Province, China).
RJ and WJ sampling was conducted between September and October 2014. Five queen-right colonies (Apis mellifera L.) were used in our experiments. RJ and WJ production were conducted in
the five colonies at the same time.
To obtain same-aged WJ and RJ samples, the
queen of each colony was confined on an empty
Figure 1. Schematic diagram of various RJ samples.
50
Y. Wang et al.
each sample type (2d-, 3d-, 4d-RJ and WJ, 5d-WJ
and O2d-, O3d- and O4d-RJ) from each colony.
We did not collect 1-day-old WJ or RJ samples, as
there is very little 1-day WJ, and the 1-day-old
larvae are too small to separate.
2.2. Analytical procedures
Moisture content was determined using a vacuum freeze-drying method (Messia et al. 2005).
Total crude protein was estimated using the
Kjeldahl method, as reported by Hoegger (1998).
The 10-HDA content was analyzed using highperformance liquid chromatography (HPLC) as defined in the national industry standard for royal jelly
(GB/T 9697–2008) of the General Administation of
Quality Supervision, Inspection and Quarantine of
the People’s Republic of China (2008). The two main
sugars of RJ and WJ (fructose and glucose) were
quantified using HPLC, as reported by Sesta (2006).
To determine levels of trace elements, approximately 0.5 g (to the nearest 0.1 mg) of the RJ and
WJ samples was first digested using a 20-mL
mixture of 4:1, HNO3: H2O2 for 24 h. The mixture
was heated to 300 °C, and when the color of the
mixture turned dark, several drops of H2O2 (30 %,
v/v) were added until it became colorless. The
solution was transferred to a 25-mL volumetric
flask and filled to volume with 5 % HNO3. Blank
digestions of non-RJ or non-WJ samples were
conducted in the same manner in order to eliminate reagent errors. The content of eight mineral
elements was determined by atomic absorption
spectroscopy (AA-6601 F; Shimadzu
Corporation, Kyoto, Japan) using the method described by Chen et al. (2006).
2.3. Statistical analysis
Before analyses were performed, Bartlett’s and
Levene’s tests were used to ensure that the data
conformed to the assumptions of ANOVA. Data
were statistically analyzed using the one-way
ANOVA procedure in SAS (version 9.1, SAS
Institute Inc. 2003; Cary, NC, USA). Duncan’s
multiple-range test was used to compare differences between means, and differences were
deemed significant at the P <0.05 level. All values
are reported as mean±SD.
3. RESULTS
The proximate composition and mineral element content of the RJ and WJ samples are shown
in Tables I and II, respectively.
The moisture content of WJ was significantly
higher than that of RJ for all 3 days (2d: F=321.5,
P <0.01; 3d: F=66.0, P <0.01; d4: F=300.6,
P <0.01) (Table I). For WJ, the moisture was
higher on 2d, 3d and 4d, but decreased rapidly
on d5 (F=110.1, P <0.01). However, unlike that of
the WJ, the moisture content of the RJ increased
with time and was significantly lower on d2
(F=31.1, P <0.01).
The proportion of total protein in the RJ was
significantly higher than that in the WJ on d2 and
d3 (2d: F=987.9, P <0.01; 3d: F=9.1, P <0.05);
however, similar protein content was found in the
d4 RJ and WJ samples (F=0.7, P >0.05). The WJ
maintained a relatively stable protein content at
d2, d3 and d4, but it decreased significantly on d5
(F=27.4, P <0.01). The protein content in the RJ
significantly decreased from d2 to d4 (F=73.1,
P <0.01).
WJ and RJ had similar trends in decreasing
proportion of 10-HDA over time; however, significant differences were found between WJ and
RJ on d2, d3 and d4 (2d: F=63.2, P <0.01; 3d:
F=12.0, P <0.05; d4: F=33.8, P <0.01). The 10HDA content of WJ was maintained at a relatively
stable level of approximately 1.50 to 1.80 % during the first 3 days, and was then reduced significantly at d4 and d5 (F=48.6, P <0.01). Although
RJ had the lowest 10-HDA content on d4, it was
still at a higher level than that of WJ.
Both the fructose and glucose levels in the RJ
were significantly higher than those for the WJ at
d2, d3 and d4 (2d: F=266.7, P <0.01; 3d: F=59.7,
P <0.05; d4: F=48.8, P <0.01 and 2d: F=43.5,
P <0.01; 3d: F=1080.5, P <0.05; d4: F=85.8,
P <0.01, respectively). In the first 3 days, the
content of fructose and glucose in the RJ was
three times that of the WJ. The food of the worker
larvae had the highest levels of fructose and glucose at d5 (F=39.3, P <0.01 and F=21.6,
P <0.01, respectively). The fructose and glucose
content of RJ were maintained at a relatively
stable level during these 3 days, despite the significantly increased fructose level on 4d (F=8.9,
2d
3d
4d
5d
O2d
O3d
O4d
Type and main wt.
(g/100 g, fresh
weight)
2d
3d
4d
5d
O2d
O3d
O4d
Type and main wt.
(g/100 g, fresh
weight)
1.06±0.050b
1.60±0.14b
2.33±0.59b
5.80±1.60a
5.12±1.03*
5.48±0.80*
6.06±0.97*
–
7.37±0.64A
5.62±0.88B
4.97±1.22B
17.93±0.27*a
14.33±1.05*b
13.73±0.44c
–
17.78±1.74A
13.39±0.84B
13.83±0.49B
RJ
1.43±0.22b
1.21±0.20b
1.60±0.11*a
1.66±0.11a
WJ
RJ
WJ
13.63±0.14a
13.91±0.45a
14.05±0.35a
11.21±0.98b
F/G
51.03±2.77b
61.55±2.40a
61.28±2.95a
–
49.01±6.59B
61.75±2.27A
61.09±3.19A
Glucose
73.22±0.10*a
72.85±0.62*a
71.73±1.11*a
57.43±3.00b
WJ
WJ
RJ
Total protein
Moisture
1.08±0.24
1.08±0.11
1.15±0.053
–
1.13±0.072A
1.09±0.10AB
1.02±0.034B
RJ
1.79±0.04a
1.78±0.14a
1.50±0.067b
0.76±0.065c
WJ
10-HDA
1.52±0.18c
1.93±0.26bc
3.70±0.70b
9.50±2.06a
WJ
2.58±0.14c
3.54±0.30bc
6.03±1.29b
15.29±3.65a
WJ
G+F
2.46±0.15A
2.29±0.54A
2.10±0.10A
3.72±0.30*a
2.58±0.15*b
2.19±0.07*c
RJ
Fructose
10.47±1.30*b
11.41±1.87*b
13.01±2.09*a
–
15.74±1.85A
11.77±2.25B
10.08±2.64B
RJ
5.35±0.37*b
5.93±1.13*b
6.95±1.15*a
–
8.37±1.23A
6.16±1.40B
5.11±1.42B
RJ
Table I. Analyzed chemical composition of the RJ and WJ samples (g/100 g, fresh weight) from different days. Data are reported as mean±SD. An asterisk (*) next to the
higher value of RJ or WJ indicates a significant difference between the RJ and WJ samples on the corresponding day at P <0.05. Different lowercase letters (a, b, c) in a
column indicate significant differences among RJ or WJ samples at P <0.05. Different uppercase letters (A, B) in a column indicate significant differences among the O2d,
O3d and O4d RJ samples at P <0.05.
Chemical composition of royal jelly and worker jelly
51
689.29±
174.75*a
673.38±
63.78*a
133.85±46.07b
3d
O4d
O3d
O2d
5d
4d
563.38±47.38a
173.39±
33.14A
170.02±
35.08A
169.69±9.72A
689.79±
31.37*a
184.10±
19.63b
191.62±
57.53b
–
1968.7±
147.42a
2126.54±
87.56a
1744.76±
228.26a
1049.82±
76.05b
WJ
RJ
WJ
17.33±0.51a
17.47±0.78a
16.72±1.85a
9.75±1.63b
K
25.43±8.55
23.66±4.44
38.04±0.90*
–
38.99±4.24A
35.63±1.37A
35.94±3.78A
Na
13.22±1.68b
16.52±3.64b
21.30±4.68b
30.73±6.66a
WJ
WJ
RJ
Zn
Fe
2d
Type and
main wt.(mg/
kg,
fresh weight)
2d
3d
4d
5d
O2d
O3d
O4d
Type and
main wt.(mg/kg,
fresh weight)
2457.16±
246.23A
1961.87±
121.81B
1977.95±
79.37B
–
2852.13±
70.27a*
2562.61±
48.83b*
1937.87±20.32c
RJ
24.80±1.32*a
24.91±3.25*a
18.23±2.59b
–
22.48±3.24A
17.56±1.61B
19.28±3.45AB
RJ
216.94±
43.34*ab
147.76±38.26b
216.94±
14.62ab
247.29±60.75a
WJ
Ca
3.88±0.30a
3.88±0.14a
3.29±0.65a
1.43±0.35b
WJ
Cu
175.97±
46.42A
217.49±
70.79A
166.92±
39.04A
257.91±
23.68a
276.29±
12.90a
108.71±
16.31b
–
RJ
4.74±0.28*a
4.66±0.38a
4.24±0.53*b
–
5.57±1.05A
3.67±0.25B
4.37±0.54B
RJ
316.22±
36.57a
343.07±
28.66ab
264.46±
56.52b
147.44±8.98c
WJ
Mg
1.87±1.51
1.49±0.62
2.37±0.18*
2.93±1.47
WJ
Mn
436.33±
21.94A
334.99±
30.95B
305.11±
15.48B
424.55±
20.28*a
337.71±
64.62a
309.92±
32.34b
–
RJ
0.52±0.16b
1.43±0.64a
1.59±0.26a
–
2.48±0.96A
0.95±0.54B
1.46±0.089AB
RJ
Table II. Mineral and trace elements in RJ and WJ samples (mg/kg, fresh weight) from different days. Data are reported as mean±SD. An asterisk (*) next to the higher
value of RJ or WJ indicates a significant difference between the RJ and WJ samples on the corresponding day at P <0.05. Different lowercase letters (a, b, c) in a column
indicate significant differences among RJ or WJ samples at P <0.05. Different uppercase letters (A, B) in a column indicate significant differences among the O2d, O3d
and O4d RJ samples at P <0.05.
52
Y. Wang et al.
Chemical composition of royal jelly and worker jelly
P <0.01). The content of F+G in RJ was significantly higher than in WJ during the first three
stages (2d: F=103.4, P <0.01; 3d: F=182.5,
P <0.01; d4: F=66.4, P <0.01). The F/G ratios
of WJ and RJ were similar at 2d and 3d (2d:
F=4.37, P =0.082; 3d: F=1.55, P =0.26). The F/G
ratio of 3d-WJ was significantly higher than that
of 3d-RJ (F=52.86, P <0.01). The F/G ratios for
4d- and 5d-WJ were significantly higher than
those for 2d- and 3d-WJ (F=6.04, P <0.05). No
significant difference was found among 2d-, 3dand 4d-RJ samples (F=0.43, P =0.66), but O2d
and O3d RJ samples had significantly higher F/G
ratios than O4d RJ (F=7.03, P <0.05).
Mineral and trace element content in the WJ
and RJ samples is shown in Table II. For the 2d
jellies, relatively high levels of zinc, copper, sodium, potassium and magnesium were found in RJ
samples compared to WJ samples. On the third
day, the RJ contained higher levels of zinc and
potassium and lower levels of sodium than the
WJ. On day 4, the content of iron and copper
was higher in RJ than in WJ, but the WJ contained
significantly higher levels of manganese, sodium
and calcium than the RJ. Most notably, zinc, copper, potassium and magnesium were found in the
lowest concentrations in 5d-WJ samples, whereas
the content of these minerals on 2d, 3d and 4d-WJ
or 2d and 3d-RJ samples was similar. The iron
content of WJ was similar during the first 3 days
and reached the highest levels at the 5d, but no
significant difference was found for the RJ samples. With time, the manganese levels in RJ were
lower on 2d and increased significantly from the
3d, but no differences were found for WJ samples.
The O2d RJ contained significantly lower
levels of moisture (F=13.14, P <0.01) and higher
levels of protein, glucose, fructose, Cu, K and Mg
than the O3d and O4d RJ samples (total protein:
F=13.14, P <0.01; glucose: F=8.44, P <0.01;
fructose: F=7.57, P <0.01; Cu: F=7.73,
P <0.01; K: F=11.95, P <0.01; and Mg:
F=39.32, P <0.01). F+G of O2d RJ was significantly higher than that of O3d RJ and O4d RJ samples
(F=8.11, P <0.01). Significant differences were
found in the content of 10-HDA, Fe, Na and Ca
among these three RJ samples (10-HDA: F=1.9,
P >0.05; Fe: F=1.21, P >0.05; Na: F=0.02,
P >0.05; and Ca: F=1.05, P >0.05). The lowest
53
levels of Zn and Mn were found in the O3d RJ
samples (Zn: F=3.32, P >0.05; and Ca: F=6.05,
P <0.05).
4. DISCUSSION
It has long been believed that caste determination in honey bees is driven by the quantity and
quality of brood food (Shuel and Dixon 1960).
Although previous research has shown that RJ
and WJ differ in some nutrients, this study showed
a more significant difference in chemical composition between RJ and WJ. We found that RJ had
lower moisture content than WJ. The WJ had high
moisture content during the first 4 days, which
decreased sharply on day 5, while an increasing
trend was found in the RJ. This is in agreement
with previous studies (Elser 1929; Smith 1959;
Dietz 1966). Elser (1929) found a decrease in the
percentage of protein in queen larvae food, and a
decreasing total protein content in RJ was also
found in our study. In a study by von Planta
(1888), higher protein and lower glucose content
was found in the food of worker larvae less than
4 days old compared with older larvae. We also
found significantly lower protein content in d5WJ and an increasing trend of glucose content in
WJ. As Kamakura (2011) found that a single
protein in royal jelly could induce queen differentiation, the royalactin content in RJ and WJ may
also differ. Although numerous studies have confirmed the 10-HDA content of RJ (Takenaka and
Echigo 1980; Lercker et al. 1992; Bloodworth
et al. 1994; Koshio and de Almeida-Muradian
2003; Zheng et al. 2011), we have found no
reports analyzing the 10-HDA content of WJ.
This study provides compelling evidence that
queen larvae are fed significantly higher amounts
of 10-HDA than are worker larvae. The 10-HDA
content in WJ was no more than 2 % during the
first 4 days, and this declined to the lowest level at
5d. Although the proportion of 10-HDA in RJ also
showed a downward trend, the 10-HDA content
remained at high levels. Previous studies found
that the proportion of sugars in RJ for female
larvae under 4 days old was approximately 34 %
(dry mass), whereas only 12 % sugars were found
in WJ fed to worker larvae 0–1.5 days old (Shuel
and Dixon 1959). Similarly, Asencot and Lensky
54
Y. Wang et al.
found that sugars in RJ for 1–3-day-old queen
larvae were at levels approximately 4 times higher
than those found in WJ (12.4 vs 3.1 %, dry mass)
(Asencot and Lensky 1988). In our study, we found
that the G+F levels in RJ were approximately 4, 3
and 2 times higher than those in WJ at d2, d3 and
d4, respectively. These results are consistent with
previous reports. Interestingly, the glucose and
fructose content in the WJ maintained low levels
at d2, d3 and d4, and increased sharply at d5. This
suggests that a higher proportion of honey is supplied to worker larvae at d5. Overall, RJ and WJ
had similar Fe, Mn, Ca and Mg content in each age
sample. The RJ contained higher levels of Zn, Cu
and K and a lower level of Na than that of WJ.
However, the Na levels in the 2d-RJ were higher,
although they were significantly lower in the O2dRJ. Because the 2d-RJ consists of 1d-RJ and O2dRJ, the additional Na content worker bees feed
female larvae the same food during their first 3 days
of larval development (Haydak 1943, 1970;
Nijhout and Wheeler 1982; Wilde and Beetsma
1982). Zheng et al. (2011) found that the composition of RJ harvested at different times varied significantly. Our results are in agreement, as RJ samples collected at 2d, 3d and 4d varied significantly.
Interestingly, when the mixture of RJ samples was
separated into each corresponding day, we found
that the composition of RJ samples fed to 3-day-old
(O3d) and 4-day-old (O4d) queen larvae was nearly identical. This may provide insight into the basic
biology of honey bees. The chemical composition
of food fed to 2-, 3- and 4-day-old worker larvae
was similar.
In mammals, gene expression and development can be influenced by nutrition (Dolinoy
et al. 2007). Previous studies have shown that
the rate of food intake is influenced by the level
of sugars (Asencot and Lensky 1975, 1976;
Lensky 1985), most likely associated with hormonally regulated mechanisms (Lensky et al.
1978; Asencot and Lensky 1984). Although
Kamakura’s work (2011) is based on the effects
of a single protein on queen differentiation, it is
unquestionably a good start in understanding the
relationship between nutrition and caste determination. In this study, tremendous variations in
chemical composition were observed between
RJ and WJ samples. We still know very little
about the role of these nutrients in honey bee caste
determination. Therefore, much still remains to be
explored of the relationship between nutritional
effects and polyphenism in honey bees.
ACKNOWLEDGMENTS
This work was financially supported by Shandong
Province Agricultural Fine Varieties Breeding Projects
(2014–2016), the earmarked fund for the China Agriculture Research System (No. CARS-45), and the National Natural Science Foundation of China (No.
31172275).
Comparaison de la composition en nutriments de la
gelée royale et de la gelée pour ouvrières chez les abeilles
( Apis mellifera )
substance chimique / valeur nutritionnelle / protéines /
fructose / glucose
Vergleich der Nährstoffzusammensetzung von
Königinnen- und Arbeiterinnenfuttersaft der
Honigbiene ( Apis mellifera )
chemische Zusammensetzung / Gelée royale /
Arbeiterinnenfuttersaft / Nahrungseffekt
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